Summary1. Our study addresses the role of non-genetic and genetic inheritance in shaping the adaptive potential of populations under a warming ocean scenario. We used a combined experimental approach [transgenerational plasticity (TGP) and quantitative genetics] to partition the relative contribution of maternal vs. paternal (additive genetic) effects to offspring body size (a key component of fitness), and investigated a potential physiological mechanism (mitochondrial respiration capacities) underlying whole-organism growth/size responses. 2. In very early stages of growth (up to 30 days), offspring body size of marine sticklebacks benefited from maternal TGP: offspring of mothers acclimated to 17°C were larger when reared at 17°C, and offspring of mothers acclimated to 21°C were larger when reared at 21°C. The benefits of maternal TGP on body size were stronger and persisted longer (up to 60 days) for offspring reared in the warmer (21°C) environment, suggesting that maternal effects will be highly relevant for climate change scenarios in this system. 3. Mitochondrial respiration capacities measured on mature offspring (F1 adults) matched the pattern of TGP for juvenile body size, providing an intuitive mechanistic basis for the maternal acclimation persisting into adulthood. Size differences between temperatures seen at early growth stages remained in the F1 adults, linking offspring body size to maternal inheritance of mitochondria. 4. Lower maternal variance components in the warmer environment were mostly driven by mothers acclimated to ambient (colder) conditions, further supporting our tenet that maternal effects were stronger at elevated temperature. Importantly, all parent-offspring temperature combination groups showed genotype 9 environment (G 9 E) interactions, suggesting that reaction norms have the potential to evolve. 5. To summarize, TGP and G 9 E interactions work in concert to mediate impacts of ocean warming on metabolic capacity and early growth of marine sticklebacks. TGP can buffer short-term detrimental effects of climate warming and may buy time for genetic adaptation to catch up, therefore markedly contributing to the evolutionary potential and persistence of populations under climate change.

Transgenerational effects can buffer populations against environmental change, yet little is known about underlying mechanisms, their persistence or the influence of environmental cue timing. We investigated mitochondrial respiratory capacity (MRC) and gene expression of marine sticklebacks that experienced acute or developmental acclimation to simulated ocean warming (21°C) across three generations. Previous work showed that acute acclimation of grandmothers to 21°C led to lower (optimized) offspring MRCs. Here, developmental acclimation of mothers to 21°C led to higher, but more efficient offspring MRCs. Offspring with a 21°C × 17°C grandmother‐mother environment mismatch showed metabolic compensation: their MRCs were as low as offspring with a 17°C thermal history across generations. Transcriptional analyses showed primarily maternal but also grandmaternal environment effects: genes involved in metabolism and mitochondrial protein biosynthesis were differentially expressed when mothers developed at 21°C, whereas 21°C grandmothers influenced genes involved in hemostasis and apoptosis. Genes involved in mitochondrial respiration all showed higher expression when mothers developed at 21° and lower expression in the 21°C × 17°C group, matching the phenotypic pattern for MRCs. Our study links transcriptomics to physiology under climate change, and demonstrates that mechanisms underlying transgenerational effects persist across multiple generations with specific outcomes depending on acclimation type and environmental mismatch between generations.

IntroductionOngoing ocean warming and acidification increasingly affect marine ecosystems, in particular around the Antarctic Peninsula. Yet little is known about the capability of Antarctic notothenioid fish to cope with rising temperature in acidifying seawater. While the whole animal level is expected to be more sensitive towards hypercapnia and temperature, the basis of thermal tolerance is set at the cellular level, with a putative key role for mitochondria. This study therefore investigates the physiological responses of the Antarctic Notothenia rossii after long-term acclimation to increased temperatures (7°C) and elevated PCO2 (0.2 kPa CO2) at different levels of physiological organisation.ResultsFor an integrated picture, we analysed the acclimation capacities of N. rossii by measuring routine metabolic rate (RMR), mitochondrial capacities (state III respiration) as well as intra- and extracellular acid–base status during acute thermal challenges and after long-term acclimation to changing temperature and hypercapnia. RMR was partially compensated during warm- acclimation (decreased below the rate observed after acute warming), while elevated PCO2 had no effect on cold or warm acclimated RMR. Mitochondrial state III respiration was unaffected by temperature acclimation but depressed in cold and warm hypercapnia-acclimated fish. In both cold- and warm-exposed N. rossii, hypercapnia acclimation resulted in a shift of extracellular pH (pHe) towards more alkaline values. A similar overcompensation was visible in muscle intracellular pH (pHi). pHi in liver displayed a slight acidosis after warm normo- or hypercapnia acclimation, nevertheless, long-term exposure to higher PCO2 was compensated for by intracellular bicarbonate accumulation.ConclusionThe partial warm compensation in whole animal metabolic rate indicates beginning limitations in tissue oxygen supply after warm-acclimation of N. rossii. Compensatory mechanisms of the reduced mitochondrial capacities under chronic hypercapnia may include a new metabolic equilibrium to meet the elevated energy demand for acid–base regulation. New set points of acid–base regulation under hypercapnia, visible at the systemic and intracellular level, indicate that N. rossii can at least in part acclimate to ocean warming and acidification. It remains open whether the reduced capacities of mitochondrial energy metabolism are adaptive or would impair population fitness over longer timescales under chronically elevated temperature and PCO2.

Antarctic notothenioid fish are characterized by their evolutionary adaptation to the cold, thermostable Southern Ocean, which is associated with unique physiological adaptations to withstand the cold and reduce energetic requirements but also entails limited compensation capacities to environmental change. This study compares the capacities of mitochondrial acclimation to ocean warming and acidification between the Antarctic nototheniid Notothenia rossii and the sub-Antarctic Lepidonotothen squamifrons, which share a similar ecology, but different habitat temperatures. After acclimation of L. squamifrons to 9°C and N. rossii to 7°C (normocapnic/hypercapnic, 0.2 kPa CO2/2000 ppm CO2) for 4–6 weeks, we compared the capacities of their mitochondrial respiratory complexes I (CI) and II (CII), their P/O ratios (phosphorylation efficiency), proton leak capacities and mitochondrial membrane fatty acid compositions. Our results reveal reduced CII respiration rates in warm-acclimated L. squamifrons and cold hypercapnia-acclimated N. rossii. Generally, L. squamifrons displayed a greater ability to increase CI contribution during acute warming and after warm-acclimation than N. rossii. Membrane unsaturation was not altered by warm or hypercapnia-acclimation in both species, but membrane fatty acids of warm-acclimated L. squamifrons were less saturated than in warm normocapnia−/hypercapnia-acclimated N. rossii. Proton leak capacities were not affected by warm or hypercapnia-acclimation of N. rossii. We conclude that an acclimatory response of mitochondrial capacities may include higher thermal plasticity of CI supported by enhanced utilization of anaplerotic substrates (via oxidative decarboxylation reactions) feeding into the citrate cycle. L. squamifrons possesses higher relative CI plasticities than N. rossii, which may facilitate the usage of energy efficient NADH-related substrates under conditions of elevated energy demand, possibly induced by ocean warming and acidification. The observed adjustments of electron transport system complexes with a higher flux through CI under warming and acidification suggest a metabolic acclimation potential of the sub-Antarctic L. squamifrons, but only limited acclimation capacities for N. rossii.